
==== Front
Sci Rep
Sci Rep
Scientific Reports
2045-2322
Nature Publishing Group UK London

39237669
70998
10.1038/s41598-024-70998-z
Article
Effect of caffeic acid and cobalt sulfate on potato (Solanum tuberosum L.) plants in the presence and absence of nanoparticles-coated urea
Danish Subhan sd96850@gmail.com

1
Hareem Misbah 2
Imran Muhammad 3
Tahir Nazia naziatahir@awkum.edu.pk

4
Gholizadeh Fatemeh 5
Datta Rahul 6
Alharbi Sulaiman Ali 7
Ansari Mohammad Javed 8
Alahmadi Tahani Awad 9
1 Pesticide Quality Control Laboratory, Agriculture Complex, Old Shujabad Road, Multan, Punjab Pakistan
2 https://ror.org/035ggvj17 grid.510425.7 0000 0004 4652 9583 Department of Environmental Sciences, Woman University Multan, Multan, Punjab Pakistan
3 Soil and Water Testing Laboratory, Khanewal, 58150 Punjab Pakistan
4 https://ror.org/03b9y4e65 grid.440522.5 0000 0004 0478 6450 Department of Agronomy, Abdul Walikhan University Mardan, Mardan, Pakistan
5 https://ror.org/05y1qcf54 grid.417760.3 0000 0001 2159 124X Department of Plant Physiology and Metabolomics, Agricultural Institute, HUN-REN Centre for Agricultural Research, Martonvásár, 2462 Hungary
6 https://ror.org/058aeep47 grid.7112.5 0000 0001 2219 1520 Department of Geology and Pedology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemedelska 1, 61300 Brno, Czech Republic
7 https://ror.org/02f81g417 grid.56302.32 0000 0004 1773 5396 Department of Botany & Microbiology College of Science King Saud University, P.O Box 2455, 11451 Riyadh, Saudi Arabia
8 https://ror.org/02e3nay30 grid.411529.a 0000 0001 0374 9998 Department of Botany, Hindu College Moradabad (Mahatma Jyotiba Phule Rohilkhand University Bareilly), Bareilly, 244001 India
9 grid.56302.32 0000 0004 1773 5396 Department of Pediatrics, College of Medicine and King, Khalid University Hospital, King Saud University, Medical City, PO Box-2925, 1146 Riyadh, Saudi Arabia
5 9 2024
5 9 2024
2024
14 206639 3 2024
23 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Potatoes (Solanum tuberosum L.) are a significant food crop cultivated around the world. Caffeic acid (CA) can enhance plant growth by promoting antioxidant activity and stimulating root development, contributing to overall plant health and vigor. Cobalt sulfate (CoSO4) boosts plant growth by promoting nitrogen (N) fixation, healthier root development, and chlorophyll synthesis, enhancing photosynthesis and overall plant health. Nanoparticle-coated urea (NPCU) improves nutrient uptake, promoting plant growth efficiency and reducing environmental impact. This study investigates the effects of combining CA, CoSO4, and NPCU as amendments on potatoes with and without NPCU. Four treatments, control, 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 with and without NPCU, were applied in four replications using a completely randomized design. Results demonstrate that the combination of CA + CoSO4 with NPCU led to an increase in potato stem length (~ 6%), shoot dry weight (~ 15%), root dry weight (~ 9%), and leaf dry weight (~ 49%) compared to the control in nutrient stress. There was a significant rise in chlorophyll a (~ 27%), chlorophyll b (~ 37%), and total chlorophyll (~ 28%) over the control under nutrient stress also showed the potential of CA + CoSO4 with NPCU. In conclusion, the findings suggest that applying CA + CoSO4 with NPCU is a strategy for alleviating potato nutrient stress.

Keywords

Chlorophyll content
Growth attributes
N-fertilizer
Solanum tuberosum L.
Subject terms

Plant sciences
Plant stress responses
Abiotic
issue-copyright-statement© Springer Nature Limited 2024
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pmcIntroduction

Nutrient deficiency can essentially affect plant growth and development1. Plants require essential nutrients, such as phosphorus (P), nitrogen (N), potassium (K), and various micronutrients, to perform key physiological processes. When these nutrients decrease in the soil, plants perform functions like photosynthesis, root development, and cell expansion2. Plants with nutrient deficiencies had smaller tubers, lower yields, and slowed growth. Certain signs indicate a lack of a nutrient, such as dark green leaves with purple discoloration for a P deficit and chlorosis of the leaves in an N shortage3. Low nutrient levels can prevent roots from growing, which limits a plant's capacity to absorb water and other necessary components. These deficiencies caused the risk of disease and pest attacks4. The growing global population and increasing food demands are putting pressure on agricultural farming and natural resources, resulting in a shortage of nutritious food and environmental effect. By 2050, a worldwide population of 9.7 billion will request 70% more food than at present consumed5. Recognizing and mitigating nutrient inadequacy is crucial for protecting soil and advancing manageable farming, meeting the nutritional requirements of a developing worldwide population6.

Caffeic acid (CA) has shown promising effects on plant growth and stress tolerance. At low concentrations (20–30 ppm), CA significantly improved growth, yield, and physiological processes in faba beans and lentils7,8. CA enhanced photosynthetic pigments, amino acids, and seed yield while reducing antinutritional factors like vicine8. In drought-stressed lentils, CA combined with ACC-deaminase-producing rhizobacteria improved plant height, pod number, and nutrient uptake while reducing stress indicators7. However, higher CA concentrations can inhibit root growth in soybeans by increasing lignification through the phenylpropanoid pathway9. Early research also demonstrated CA growth-promoting activity in pea epicotyl straight growth tests10.

Cobalt has been shown to enhance nitrogen uptake and utilization in plants, particularly legumes. Studies on pea11, cowpea12, and soybean13 demonstrated that cobalt application increased plant growth, yield, and nutrient content, especially nitrogen. Cobalt's role in improving nitrogen fixation efficiency is attributed to its essential function in vitamin B12 synthesis, required by enzymes involved in N2 fixation14. The optimal cobalt concentration for plant growth varies, with 8 ppm for pea11, 7.5 ppm for cowpea12 , and 12 mg/kg for soybean showing the best results13. However, excessive cobalt can be toxic to plants14. Adding cobalt can reduce the required nitrogen fertilizers while maintaining or improving plant growth and yield11–13.

Applying nanoparticle-coated urea enhances plant growth by facilitating efficient nutrient uptake and utilization15. The nanoparticles serve as carriers, gradually releasing urea, which promotes sustained nutrient availability to plants16. This controlled release mechanism minimizes N loss through leaching or volatilization, maximizing plant nutrient absorption. Incorporating silica nanoparticles into polyacrylate emulsions for urea coating has been shown to extend nutrient release duration and improve wear resistance17–19. Consequently, plants exhibit improved physiological processes, including enhanced photosynthesis, increased biomass accumulation, and heightened resistance to environmental stressors20.

Potato (Solanum tuberosum L.) ranks as one of the most widely cultivated vegetable crops globally, with a presence in 79% of countries worldwide21. It is fourth in production volume, followed by rice, wheat, and maize. Potatoes are a valuable source of affordable and readily available proteins, essential amino acids, carbohydrates, minerals, antioxidants, and vitamins globally22. Nutrient deficiency in potatoes leads to stunted growth, reduced yield, and poor-quality tubers. Potatoes need a balanced supply of N, P, K, and micronutrients. Addressing these deficiencies through appropriate fertilization strategies is crucial for optimal growth and yield.

That’s why the present study was planned to investigate the influence of CA and CoSO4 in combination with NPCU on potato growth cultivated in N-deficient soil. This study examines the individual and combined effects of CA and CoSO4 with and without NPCP on the growth of potato plants in N-deficient soil. The study covers the knowledge gap regarding the sole and combined use of CA and CoSO4 with and without NPCU for the improvement in the growth of potato plants. Compared to the control, potato growth might be improved in N-deficient soils by applying CA and CoSO4 with NPCU.

Material and methods

Experimental site

In 2022, a pot experiment was conducted in the experimental area of ResearchSolution (30°09′41.6″N 71°36′38.0″E). During the experiment conduction, the temperature was maintained at 25–30 °C. Humidity was maintained at 60–70%. The day sunlight exposure was 6–8 h. Random soil sampling was done from the research area to characterize soil physicochemical properties. The soil and irrigation water parameters before experimentation were given in Table 1. Table 1 Pre-experimental soil and irrigation characteristics.

Soil	Values	Water	Values	
pH	8.16	pH	7.27	
ECe (dS/m)	3.13	ECe (µS/cm)	241	
Soil organic matter (%)	0.42	Carbonates (meq/L)	0.05	
Total N (%)	0.001	Bicarbonates (meq/L)	4.12	
Extractable P (mg/kg)	5.13	Chloride (meq/L)	0.00	
Available K (mg/kg)	103	Ca + Mg (meq/L)	3.17	
Silt (%)	46	Sodium (mg/L)	63	
Sand (%)	24	Ca + Mg = Calcium + Magnesium

CEC = Cation exchange capacity

ECe = Electrical conductivity

	
Clay (%)	30	
Texture	Clay Loam	

Nanoparticles coated urea

A standard protocol23 was utilized to synthesize Urea-covered nanoparticles, integrating specific modifications. Polyvinyl alcohol (PVA) was chosen as the coating material due to its stable ecological compatibility, biocompatibility, and film-framing properties. The surface of a single superphosphate was treated with a solution of 10 mg ZnO nanoparticles and PVA (7%) 24 and coated urea dried at ambient temperature to create a durable PVA coating layer.

Experimental design and treatment plan

In this experiment, a fully randomized design (CRD) was used to deliver four treatments in four replicates: control, caffeic Acid (20 µM CA), cobalt sulfate (0.15 mg/L CoSO4), and 20 µM CA + 0.15 mg/L CoSO4. Nanoparticles-coated urea (NPCU) (5 mg ZnO NP/kg soil) was mixed in the soil during soil preparation for pot filling. However, CA and CoSO4 foliar application were done in 2 splits. The first foliar was done after three weeks of germination, while the second was done before tuber initiation (42 days after germination).

Seed collection, sowing, and thinning

For experimental purposes, the potato variety Sahiwal White (FD 73–110) was sown in 2nd fortnight of October. Each pot filled with 10 kg of soil was then sown with seventeen seeds. Two seedlings in each pot were maintained by thinning after germination.

Fertilizer

To meet the nutritional needs of potatoes, we implemented a N application at a rate of 247 kg per ha (equivalent to around 0.31 g/10 kg soil) obtained from urea. Simultaneously, P was introduced at a rate of 124 kg per ha (almost 0.15 g/10 kg soil), sourced from a single superphosphate, by recommended application protocols. Additionally, to enhance K levels, we augmented the soil with 124 kg per acre of K sulfate (about 0.15 g/10 kg soil). In the control plant, simple urea was added, but there was no nanoparticle coating. All fertilizers were applied in the soil during soil preparation for pot filling.

Irrigation

The irrigation control for individual pots was meticulously handled using a moisture indicator (ADVANCED™; 4 in 1 Soil Meter; China). Regular monitoring and daily supervision were conducted to maintain moisture levels within the specified range, ensuring 70% of the soil field capacity was maintained.

Harvesting and collection of data

After 65 days of sowing, harvesting was performed for data collection (tuber bulking stage). The fresh weight of samples was assessed using digital balance soon after harvesting. For dry weight assessment, samples were oven-dried for 72 h at 65 °C.

Chlorophyll contents and gas exchange attributes

To assess the chlorophyll contents in freshly harvested leaf samples, we ground the samples with 5 ml of 80% acetone24. After that filtration was done to remove the plant tissue residues. The absorbance of the aliquot was assessed at 645, 663 nm, and 480 nm wavelength using a UV-spectrophotometer (Multipurpose Shimadzu UV-1280)25. Using a CI-340 photosynthesis instrument to measure gas exchange attributes including intercellular CO2, leaf stomatal conductance, and net transpiration rate26. Fully expanded leaves were placed in the clip during the sunny morning from 10:45 to 11:35 AM, and readings of attributes were recorded.

Total soluble sugar, protein, and free proline

The method proposed by27 was used for assessing total sugar content using anthrone and 80% H2SO4, subjected to a 10-min water bath, heated and cooled, and measured optical density at 620 nm using a UV-spectrophotometer (Multipurpose Shimadzu UV-1280). Fresh leaf samples were standardized with 50 mM K phosphate buffer, centrifuged at 10,000×g for 15 min at 4 °C, and protein concentration in the extract was measured using the method of28. The glacial acetic acid, ninhydrin solutions, and sulfosalicylic acid were used to measure free proline content, following protocol29. The combined solution was heated at 100 °C, and 5 ml of toluene was added. Subsequently, the absorbance was recorded at 520 nm.

Antioxidants

Using the protocol outlined by30, the amount of superoxide dismutase (SOD) was measured by observing the decrease of nitro blue tetrazolium (NBT) at 560 nm. At 420 nm, peroxidase (POD) activity was measured31. The activity of catalase (CAT) was assessed by measuring the decrease in absorbance at 240 nm, which results in the breakdown of hydrogen peroxide (H2O2) Aebi (1984). Following the protocol, Ascorbate peroxidase (APX) activity was calculated by checking ascorbate oxidation in the presence of H2O2 at 290 nm. The study determined Malondialdehyde (MDA) levels by reacting the sample extract with thiobarbituric acid (TBA), forming a colored complex, and measuring its absorbance at 532 nm32.

Free proline determination

N, P, K, and Ca in leave

Initially, N sulfuric acid33 and P and K di-acid mixture34 were used for digestion. To assess N content using glass Kjeldahl’s distillation apparatus standard method was followed35. The P content was assessed at 420 nm using protocol35. A flame photometer (microprocessor-1385) was used to quantify K and Ca content36,37.

Statistical analysis

The data was subjected to standard statistical analysis38. A two-way ANOVA was applied using OriginPro 2024b (64-bit) software; 10.1.5.132. The paired comparison was done for making graphs and statistical lettering on bars at p ≤ 0.05 using the Tukey test. Convex hull and hierarchical cluster analysis examined the best treatment and most representable attribute using OriginPro 2024b (64-bit) software; 10.1.5.13239.

Results

Stem length, shoot, root, and leaf dry weight

Applying 20 μM CA, 0.15 mg/L CoSO4 and 20 μM CA + 0.15 mg/L CoSO4 with no nanoparticle resulted increase in stem length (~ 8%, ~ 3%, and ~ 11%), shoot dry weight (~ 12%, ~ 4%, and ~ 19%), root dry weight (~ 4%, ~ 3%, and ~ 10%), and leaf dry weight (~ 47%, ~ 15%, and ~ 79%) than the control. Treatment 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 with NPCU caused a rise in stem length (~ 4%, ~ 3%, and ~ 6%), shoot dry weight (~ 11% ~ 8%, and ~ 15%), root dry weight (~ 5%, ~ 4%, and ~ 9), and leaf dry weight (~ 32%, ~ 11%, and ~ 49%) over the control (Fig. 1A–D).Fig. 1 Effect of caffeic acid (CA), cobalt sulfate (CoSO4), and nanoparticle coated urea (NPCU) on stem length (A), shoot dry weight (B), root dry weight (C) and leaf dry weight (D) concentration of leaves of potatoes. The Tukey test measured significant differences (p ≤ 0.05); distinct letters on the bars are the mean of four replicates ± SE.

Chlorophyll content and carotenoids

A significant increase in chlorophyll a (~ 46%, ~ 25%, and ~ 58%), chlorophyll b (~ 21%, ~ 70% ~ 46%), total chlorophyll (~ 46%, ~ 26%, and ~ 61%), and carotenoids (~ 42%, ~ 18%, and ~ 61%) were recorded than the control. Applying 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 treatments exhibit an increase in chlorophyll a (~ 18%, ~ 8%, and ~ 27%) chlorophyll b (~ 19%, ~ 80%, and ~ 45), total chlorophyll (~ 17%, ~ 7%, and ~ 28%), and carotenoids (~ 21%, ~ 10%, and ~ 30%) from the control under NPCU (Fig. 2A–D).Fig. 2 Effect of caffeic acid (CA), cobalt sulfate (CoSO4), and nanoparticle coated urea (NPCU) on chlorophyll a (A), chlorophyll b (B), total chlorophyll (C) and carotenoid (D) concentration of leaves of potatoes. The Tukey test measured significant differences (p ≤ 0.05); distinct letters on the bars are the mean of four replicates ± SE.

Gas exchange attributes

By adding 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 treatment showed an increase in photosynthetic rate (~ 13%, ~ 54%, and ~ 32%), stomatal conductance (~ 37%, ~ 22%, and ~ 52%), transpiration rate (~ 29%, ~ 13%, and 41%), and intercellular CO2 concentration (~ 49%, ~ 42%, and ~ 99%) under no NP than the control. Applying 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 treatment with NPCU showed a maximum increase in photosynthetic rate (~ 14%, ~ 59%, and ~ 45%), stomatal conductance (~ 20%, ~ 11%, and ~ 27%), transpiration rate (~ 35%, ~ 23%, and ~ 42%), and intercellular CO2 concentration (~ 82%, ~ 31%, and ~ 97%) compared to the control (Fig. 3A–D).Fig. 3 Effect of caffeic acid (CA), cobalt sulfate (CoSO4), and nanoparticle coated urea (NPCU) on photosynthetic rate (A), stomatal conductance (B), transpiration rate (C) and intercellular CO2 rate (D) concentration of leaves of potatoes. The Tukey test measured significant differences (p ≤ 0.05); distinct letters on the bars are the mean of four replicates ± SE.

Total soluble protein, soluble sugar, and free amino acid

Contrast to the control, treatments 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 with no nanoparticle showed a rise in total soluble protein (~ 41%, ~ 21%, and ~ 62%), soluble sugar (~ 32%, ~ 18%, and ~ 53%), and free amino acid (~ 44%, ~ 20%, and ~ 69%). Applying of NPCU with 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 resulted an increase in total soluble protein (~ 22%, ~ 10%, and ~ 30%), soluble sugar (~ 22%, ~ 14%, and ~ 30%), and free amino acid (~ 26%, ~ 14%, and ~ 38%) over the control (Fig. 4A–C).Fig. 4 Effect of caffeic acid (CA), cobalt sulfate (CoSO4), and nanoparticle coated urea (NPCU) on total soluble sugar (A), soluble protein (B) and free amino acid (C) concentration of leaves of potatoes. The Tukey test measured significant differences (p ≤ 0.05); distinct letters on the bars are the mean of four replicates ± SE.

H2O2, MDA, and POD

A significant decrease in H2O2 content (~ 8%, 5%, and 13%), MDA (~ 15%, ~ 7%, and ~ 29%), and POD (~ 12%, ~ 7%, and ~ 24%) activity were observed by adding 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 treatment under no NPCU than the control. NPCU with 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 resulted significant decrease in H2O2 content (~ 27%, ~ 28%, and ~ 99%), MDA (~ 25%, ~ 15%, and ~ 64%), and POD (~ 13% ~ 9, and ~ 51%) activity than the control (Fig. 5A–C).Fig. 5 Effect of caffeic acid (CA), cobalt sulfate (CoSO4), and nanoparticle coated urea (NPCU) on H2O2 (A), MDA (B) and POD (C) concentration of leaves of potatoes. The Tukey test measured significant differences (p ≤ 0.05); distinct letters on the bars are the mean of four replicates ± SE.

SOD, CAT, and proline

By adding 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 treatment showed a decrease in SOD (~ 12%, 7%, and ~ 28%), CAT (~ 13%, ~ 6%, and ~ 32%), and proline (~ 20%, ~ 16%, and ~ 38%) under no NP from the control. Applying 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 treatment with NPCU showed a maximum decrease in SOD (~ 32%, ~ 18%, and ~ 68%), CAT (~ 34%, ~ 27%, and ~ 77%), and proline (~ 17%, ~ 6%, and ~ 21%) in contrast to the control (Fig. 6A–C).Fig. 6 Effect of caffeic acid (CA), cobalt sulfate (CoSO4), and nanoparticle coated urea (NPCU) on CAT (A), proline content (B) and SOD (C) concentration of leaves of potatoes. The Tukey test measured significant differences (p ≤ 0.05); distinct letters on the bars are the mean of four replicates ± SE.

N, P, K, and Ca in leaves

Adding 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 with no NP caused an increase in leave N (~ 2%, ~ 1%, and ~ 3%), leave P (~ 56%, ~ 26%, and ~ 97%), leave K (~ 12%, ~ 5%, and ~ 17%), and leave Ca (~ 6%, ~ 3%, and ~ 10%) compared to control. Increase in leaves N (~ 3%, ~ 2%, and ~ 3%), leave P (~ 25%, ~ 13%, and ~ 33%), leave K (~ 7%, ~ 7%, and ~ 21%), and leave Ca (~ 6%, ~ 4%, and ~ 12%) by applying 20 μM CA, 0.15 mg/L CoSO4, and 20 μM CA + 0.15 mg/L CoSO4 treatment with NPCU contrast to the control (Table 2). Table 2 Effect of caffeic acid (CA), cobalt sulfate (CoSO4), and nanoparticle coated urea (NPCU) on N, P, K, and Ca concentration of leaves of potatoes.

Treatment	Leave N (%)	Leave P (%)	Leave K (%)	Leave Ca (%)	
	No NP	
Control	3.65f	1.62 g	3.16f	0.40e	
20 μM CA	3.73de	2.40e	3.54de	0.43d	
0.15 mg/L CoSO4	3.70e	2.00f	3.31ef	0.41de	
20 μM CA + 0.15 mg/L CoSO4	3.77d	3.12d	3.70 cd	0.44c	
	NPCU	
Control	3.84c	3.54c	3.88bc	0.45c	
20 μM CA	3.94ab	4.41a	4.15b	0.48b	
0.15 mg/L CoSO4	3.91b	3.99b	4.15b	0.47b	
20 μM CA + 0.15 mg/L CoSO4	3.95a	4.72a	4.71a	0.50a	

The Tukey test measured significant differences (p ≤ 0.05); distinct letters on the bars are the mean of four replicates ± SE.

Convex hull and hierarchical cluster analysis

The control group demonstrates scores clustered around negative values on PC 1, with varying scores on PC 2, ranging from − 7.88126 to 1.62146. In contrast, the treatment group administered with 20 μM CA shows scores distributed across PC 1 and PC 2, ranging from − 3.99695 to 6.10181. Similarly, the treatment group exposed to 0.15 mg/L CoSo4 displays a spread of scores from -5.77306 to 4.31424. The combination treatment of 20 μM CA and 0.15 mg/L CoSo4 exhibits scores extending from − 2.17416 to 8.21149, showing a distinct pattern compared to individual treatments (Fig. 7A).Fig. 7 Convex Hull cluster plots for treatments (A), NP levels (B), and Hierarchical Cluster analysis (C) for the studied attributes.

With Principal Component (PC) 1 explaining the vast majority of variance at 96.76%, it emerges as the dominant factor shaping the dataset's structure. Meanwhile, PC 2 contributes a minor 1.16% to the overall variance. Different treatment response patterns are presented by examining the treatment scores and distinct clusters. Most data points cluster tightly under the label no NP, indicated by negative values on PC 1 and positive values on PC 2, suggesting a consistent treatment response within this subgroup. In contrast, another cluster labeled NPCU exhibits positive values on PC 1 and PC 2, indicating a distinct treatment response pattern (Fig. 7B).

The analysis reveals clusters of variables based on their similarities. For instance, variables such as total soluble sugar and free amino acids exhibit a similarity of 0.0816, suggesting a close association in their properties. Similarly, chlorophyll a and total chlorophyll are similar to 0.1404, indicating a related nature. Soluble protein and leaf dry weight, photosynthetic rate, and leaf dry weight form clusters with similarities of 0.14656 and 0.23607, respectively, implying shared characteristics within each cluster. Furthermore, the analysis highlights significant associations among variables such as shoot dry weight and leaf N percentage, which exhibit a high similarity of 0.25467, suggesting a strong relationship between these parameters. Stomatal conductance and transpiration rate also exhibit a substantial resemblance of 0.27344, showing their close correlation in plant physiology.

Interestingly, variables such as stem length and leaf K percentage display a similarity of 0.6761 and 0.71185, respectively, suggesting a significant association between these parameters. Additionally, the analysis identifies variables such as H2O2 and intercellular CO2 rate, which exhibit higher similarities of 1.83681 and 2.21367, respectively, indicating potential physiological relationships between these parameters. The analysis concludes with variables such as SOD and chlorophyll b, which show similarities of 3.65837 and 7.91511, respectively, suggesting distinct characteristics within the dataset (Fig. 7C).

Pearson correlation analysis

Variables like stem length, shoot, root, and leaf dry weight exhibit strong positive correlations ranging from 0.97256 to 0.98804, revealing their close connection with plant development and biomass accumulation. Furthermore, chlorophyll-related parameters, including chlorophyll a, b, total, and carotenoid content, demonstrate high positive correlations, ranging from 0.83071 to 0.99724, highlighting the interconnectedness of these pigment-related processes in photosynthesis and plant metabolism. The photosynthetic rate, stomatal conductance, and transpiration rate also exhibit strong positive correlations with values ranging from 0.94456 to 0.99551, suggesting their synchronized roles in gas exchange and carbon assimilation within plant tissues. Conversely, oxidative stress-related parameters such as H2O2, MDA, POD, SOD, and CAT demonstrate adverse relationships with other variables, representing their inverse relationships. For instance, H2O2 and MDA exhibit negative correlations with most variables, suggesting their roles as indicators of oxidative stress levels in plants. Additionally, parameters related to leaf N, P, and K percentages demonstrate positive correlations, ranging from 0.81827 to 0.99337, reflecting their interconnected roles in plant nutrient uptake and metabolism (Fig. 8).Fig. 8 Pearson correlation analysis for the studied attributes.

Discussion

Caffeic acid

Caffeic acid has been shown to improve nitrogen uptake and utilization in plants, particularly under stress conditions. It can stimulate net nitrogen uptake at low concentrations40 and mitigate the adverse effects of abiotic stresses in plants by enhancing improving antioxidant activity41. Improving nitrogen use efficiency through altered amino acid transport processes can lead to increased biomass and seed yields, even in nitrogen-poor soils42. Plants can directly absorb amino acids, bypassing the mineralization step and potentially accelerating nitrogen turnover43. This ability varies among species, with deciduous shrubs and ectomycorrhizal species generally showing higher amino acid uptake rates43. These findings suggest that caffeic acid and related compounds play a crucial role in enhancing plant nitrogen uptake and overall stress tolerance. Hierarchical cluster analysis in current study also in agreement of above arguments. It clearly showed that free amino acids improvement in current study was the most representable attribute that played a crucial role in improvement of potato growth in N deficient soil.

Cobalt

Cobalt plays a crucial role in enhancing nitrogen uptake and improving plant growth across various crops. Studies on pea, cowpea, and groundnut have shown that cobalt application significantly increases nodule formation, nitrogenase activity, and nitrogen fixation efficiency11,44,45. Cobalt supplementation allows for a 25% reduction in nitrogen fertilizer use while maintaining or improving crop yields and quality11,44,45. The element enhances the uptake of macronutrients (N, P, K) and micronutrients (Mn, Zn), although it may reduce iron content due to antagonistic relationships46. Cobalt application results in increased plant growth parameters, improved pod and seed yields, and enhanced chemical composition of crops46,47. These findings suggest that cobalt supplementation can optimize nitrogen fertilization efficiency, reduce environmental pollution from excess nitrogen, and potentially lower agricultural costs for farmers.

Nanoparticle-coated urea

Nanoparticles can boost photosynthetic rate, biomass, chlorophyll content, and upregulate stress-related genes in plants48. Nanoparticle-coated urea has shown promising results in improving nitrogen uptake and enhancing crop performance. Fe3O4-urea nanocomposites significantly increased photosynthetic efficiency, nitrogen metabolism, and crop yield in rice49. Similarly, ZnO nanoparticle-coated urea improved wheat performance under drought stress, enhancing grain yield and zinc uptake50. Zinc oxide nanoparticle-coated urea also demonstrated superior results in terms of slow nutrient release, nitrogen and zinc uptake, and grain yield in wheat compared to uncoated urea51.

Conclusion

In conclusion, treatment 20 μM CA + 0.15 mg/L CoSO4 with NPCU can improve potato growth in N deficient soil. Application of 20 μM CA + 0.15 mg/L CoSO4 with NPCU can improve free amino acids, chlorophyll content, and uptake of macronutrients (i.e., N, P and K) that act as key factors for potato growth enhancement. Growers are recommended to apply 20 μM CA + 0.15 mg/L CoSO4 with NPCU for better growth and uptake of nutrients in potato in N deficient soils compared to simple urea application. More investigations are recommended at field levels to declare 20 μM CA + 0.15 mg/L CoSO4 with NPCU as most efficacious amendment for improvement of potato growth in different agro climates soils.

Acknowledgements

This project was supported by Researchers Supporting Project number (RSP2025R230) King Saud University, Riyadh, Saudi Arabia.

Author contributions

Conceptualization; M.H.; S.D.; N.T.; F.G.; Conducted experiment; S.D.; M.H.; M.I.; Formal analysis; M.H.; M.I.; Methodology; N.A.; R.D.; N.T.; F.G.; Writing—original draft; M.J.A.; S.D.; S.A.A.; T.A.A.; Writing—review & editing; M.J.A.; R.D.; S.A.A.; T.A.A.

Funding

This project was supported by Researchers Supporting Project number (RSP2025R230) King Saud University, Riyadh, Saudi Arabia.

Data availability

All data generated or analysed during this study are included in this published article.

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

We all declare that manuscript reporting studies do not involve any human participants, human data, or human tissue. So, it is not applicable. Experimental research and field studies on plants (either cultivated or wild), including the collection of plant material, must comply with relevant institutional, national, and international guidelines and legislation. We confirmed that all methods were performed in accordance with the relevant guidelines/regulations/legislation. The seeds were purchased from a local certified seed dealer of the Government of Punjab, Pakistan.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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References

1. Kumar S Abiotic stresses and their effects on plant growth, yield and nutritional quality of agricultural produce Int. J. Food Sci. Agric 2020 4 367 378
Kumar, S. Abiotic stresses and their effects on plant growth, yield and nutritional quality of agricultural produce. Int. J. Food Sci. Agric 4, 367–378 (2020).
2. Ameen, M. et al. Nutrient acquisition, transport and metabolism within the plant cells. In Sustainable plant nutrition 51–70 (Elsevier, 2023).
3. Lommen WJM Environmental conditions after planting affect the expression of differences in tuber formation of in vitro-derived potato plantlets from different ages and cultivars Potato Res. 2023 67 1 117 137 10.1007/s11540-023-09622-y
Lommen, W. J. M. Environmental conditions after planting affect the expression of differences in tuber formation of in vitro-derived potato plantlets from different ages and cultivars. Potato Res. 67(1), 117–137 (2023).10.1007/s11540-023-09622-y
4. Bethke, P. C. & Jansky, S. H. Genetic and environmental factors contributing to reproductive success and failure in potato. Am. J. Potato Res. 98, 24–41 10.1007/s12230-020-09810-3 (2021).
5. Zarzyńska K Trawczyński C Pietraszko M Environmental and agronomical factors limiting differences in potato yielding between organic and conventional production system Agriculture 2023 13 4 901 10.3390/agriculture13040901
Zarzyńska, K., Trawczyński, C. & Pietraszko, M. Environmental and agronomical factors limiting differences in potato yielding between organic and conventional production system. Agriculture 13(4), 901 (2023).10.3390/agriculture13040901
6. Saeed R Tea [Camellia sinensis (L.) kuntze] leaf compost ameliorates the adverse effects of salinity on growth of cluster beans (Cyamopsis tetragonoloba L.) Pak. J. Bot. 2016 48 495 501
Saeed, R. et al. Tea [Camellia sinensis (L.) kuntze] leaf compost ameliorates the adverse effects of salinity on growth of cluster beans (Cyamopsis tetragonoloba L.). Pak. J. Bot. 48, 495–501 (2016).
7. Zafar-ul-Hye M Rhizobacteria inoculation and caffeic acid alleviated drought stress in lentil plants Sustainability 2021 13 9603 10.3390/su13179603
Zafar-ul-Hye, M. et al. Rhizobacteria inoculation and caffeic acid alleviated drought stress in lentil plants. Sustainability 13, 9603 (2021).10.3390/su13179603
8. El-Awadi ME Investigations of growth promoting activity of some phenolic acids Agric. Eng. Int. CIGR J. 2017 19 53 60
El-Awadi, M. E. Investigations of growth promoting activity of some phenolic acids. Agric. Eng. Int. CIGR J. 19, 53–60 (2017).
9. Bubna GA Exogenous caffeic acid inhibits the growth and enhances the lignification of the roots of soybean (Glycine max) J. Plant Physiol. 2011 168 1627 1633 10.1016/j.jplph.2011.03.005 21489652
Bubna, G. A. et al. Exogenous caffeic acid inhibits the growth and enhances the lignification of the roots of soybean (Glycine max). J. Plant Physiol. 168, 1627–1633 (2011).21489652 10.1016/j.jplph.2011.03.005
10. Vendrig JC Buffel K Growth-promoting activity of caffeic acid Nature 1962 193 1204 1204 10.1038/1931204a0 13922819
Vendrig, J. C. & Buffel, K. Growth-promoting activity of caffeic acid. Nature 193, 1204–1204 (1962).13922819 10.1038/1931204a0
11. Gad N Increasing the efficiency of nitrogen fertilization through cobalt application to pea plant Res. J. Agric. Biol. Sci. 2007 2 433 442
Gad, N. Increasing the efficiency of nitrogen fertilization through cobalt application to pea plant. Res. J. Agric. Biol. Sci. 2, 433–442 (2007).
12. Siam HS Mahmoud A Abdel Hady M Increasing the utilization efficiency of nitrogenous fertilizers by cobalt addition and its effect on growth, yield parameters and nutrients contents of cowpea plants J. Appl. Sci. Res. 2012 8 2 915 929
Siam, H. S., Mahmoud, A. & Abdel Hady, M. Increasing the utilization efficiency of nitrogenous fertilizers by cobalt addition and its effect on growth, yield parameters and nutrients contents of cowpea plants. J. Appl. Sci. Res. 8(2), 915-929 (2012).
13. Kandil HM Farid IM el-Maghraby AM Effect of cobalt level and nitrogen source on quantity and quality of soybean plant J. Appl. Sci. Res. 2013 8 2 915 929
Kandil, H. M., Farid, I. M. & el-Maghraby, A. M. Effect of cobalt level and nitrogen source on quantity and quality of soybean plant. J. Appl. Sci. Res. 8(2), 915–929 (2013).
14. Hu X Wei X Ling J Chen J Cobalt: an essential micronutrient for plant growth? Front Plant. Sci. 2021 12 768523 10.3389/fpls.2021.768523 34868165
Hu, X., Wei, X., Ling, J. & Chen, J. Cobalt: an essential micronutrient for plant growth? Front Plant. Sci. 12, 768523 (2021).34868165 10.3389/fpls.2021.768523
15. Xin X Judy JD Sumerlin BB He Z Nano-enabled agriculture: from nanoparticles to smart nanodelivery systems Environ. Chem. 2020 17 413 10.1071/EN19254
Xin, X., Judy, J. D., Sumerlin, B. B. & He, Z. Nano-enabled agriculture: from nanoparticles to smart nanodelivery systems. Environ. Chem. 17, 413 (2020).10.1071/EN19254
16. Amin S Zinc oxide nanoparticles coated urea enhances nitrogen efficiency and zinc bioavailability in wheat in alkaline calcareous soils Environ. Sci. Pollut. Res. 2023 30 70121 70130 10.1007/s11356-023-27209-5
Amin, S. et al. Zinc oxide nanoparticles coated urea enhances nitrogen efficiency and zinc bioavailability in wheat in alkaline calcareous soils. Environ. Sci. Pollut. Res. 30, 70121–70130 (2023).10.1007/s11356-023-27209-5
17. Elhassani, C. E. et al. Lignin nanoparticles filled chitosan/polyvinyl alcohol polymer blend as a coating material of urea with a slow‐release property. J. Appl. Polym. Sci. 140, (2023).
18. Shen Y Zhou J Du C Development of a polyacrylate/silica nanoparticle hybrid emulsion for delaying nutrient release in coated controlled-release urea Coatings 2019 9 88 10.3390/coatings9020088
Shen, Y., Zhou, J. & Du, C. Development of a polyacrylate/silica nanoparticle hybrid emulsion for delaying nutrient release in coated controlled-release urea. Coatings 9, 88 (2019).10.3390/coatings9020088
19. Beig, B. et al. Development and testing of zinc sulfate and zinc oxide nanoparticle-coated urea fertilizer to improve N and Zn use efficiency. Front. Plant Sci. 13, (2023).
20. Pramanik A Nanocatalyst-based biofuel generation: an update challenges and future possibilities Sustainability 2023 15 6180 10.3390/su15076180
Pramanik, A. et al. Nanocatalyst-based biofuel generation: an update challenges and future possibilities. Sustainability 15, 6180 (2023).10.3390/su15076180
21. De Vrieze M Germanier F Vuille N Weisskopf L Combining different potato-associated pseudomonas strains for improved biocontrol of phytophthora infestans Front. Microbiol. 2018 9 2573 10.3389/fmicb.2018.02573 30420845
De Vrieze, M., Germanier, F., Vuille, N. & Weisskopf, L. Combining different potato-associated pseudomonas strains for improved biocontrol of phytophthora infestans. Front. Microbiol. 9, 2573 (2018).30420845 10.3389/fmicb.2018.02573
22. Chourasia KN Salinity stress in potato: understanding physiological, biochemical and molecular responses Life 2021 11 545 10.3390/life11060545 34200706
Chourasia, K. N. et al. Salinity stress in potato: understanding physiological, biochemical and molecular responses. Life 11, 545 (2021).34200706 10.3390/life11060545
23. Klimczyk M Siczek A Schimmelpfennig L Improving the efficiency of urea-based fertilization leading to reduction in ammonia emission Sci. Total Environ. 2021 771 145483 10.1016/j.scitotenv.2021.145483 33736136
Klimczyk, M., Siczek, A. & Schimmelpfennig, L. Improving the efficiency of urea-based fertilization leading to reduction in ammonia emission. Sci. Total Environ. 771, 145483 (2021).33736136 10.1016/j.scitotenv.2021.145483
24. Arnon DI Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris Plant Physiol. 1949 24 1 10.1104/pp.24.1.1 16654194
Arnon, D. I. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1 (1949).16654194 10.1104/pp.24.1.1
25. Kirk JTO Allen RL Dependence of chloroplast pigment synthesis on protein synthesis: Effect of actidione Biochem. Biophys. Res. Commun. 1965 21 523 530 10.1016/0006-291X(65)90516-4 5879460
Kirk, J. T. O. & Allen, R. L. Dependence of chloroplast pigment synthesis on protein synthesis: Effect of actidione. Biochem. Biophys. Res. Commun. 21, 523–530 (1965).5879460 10.1016/0006-291X(65)90516-4
26. Nazar R Khan MIR Iqbal N Masood A Khan NA Involvement of ethylene in reversal of salt-inhibited photosynthesis by sulfur in mustard Physiol. Plant. 2014 152 331 344 10.1111/ppl.12173 24547902
Nazar, R., Khan, M. I. R., Iqbal, N., Masood, A. & Khan, N. A. Involvement of ethylene in reversal of salt-inhibited photosynthesis by sulfur in mustard. Physiol. Plant. 152, 331–344 (2014).24547902 10.1111/ppl.12173
27. Yemm, E. W. & Willis, A J. The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57, 508–514 (1954).
28. Bradford MM A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976 72 248 254 10.1016/0003-2697(76)90527-3 942051
Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).942051 10.1016/0003-2697(76)90527-3
29. Bates LS Waldren RP Teare ID Rapid determination of free proline for water-stress studies Plant Soil 1973 39 205 207 10.1007/BF00018060
Bates, L. S., Waldren, R. P. & Teare, I. D. Rapid determination of free proline for water-stress studies. Plant Soil 39, 205–207 (1973).10.1007/BF00018060
30. Hori M Changes in the hepatic glutathione peroxidase redox system produced by coplanar polychlorinated biphenyls in Ah-responsive and-less-responsive strains of mice: Mechanism and implications for toxicity Environ. Toxicol. Pharmacol. 1997 3 267 275 10.1016/S1382-6689(97)00025-2 21781787
Hori, M. et al. Changes in the hepatic glutathione peroxidase redox system produced by coplanar polychlorinated biphenyls in Ah-responsive and-less-responsive strains of mice: Mechanism and implications for toxicity. Environ. Toxicol. Pharmacol. 3, 267–275 (1997).21781787 10.1016/S1382-6689(97)00025-2
31. Dhindsa RS Plumb-Dhindsa PL Reid DM Leaf senescence and lipid peroxidation: Effects of some phytohormones, and scavengers of free radicals and singlet oxygen Physiol. Plant 1982 56 453 457 10.1111/j.1399-3054.1982.tb04539.x
Dhindsa, R. S., Plumb-Dhindsa, P. L. & Reid, D. M. Leaf senescence and lipid peroxidation: Effects of some phytohormones, and scavengers of free radicals and singlet oxygen. Physiol. Plant 56, 453–457 (1982).10.1111/j.1399-3054.1982.tb04539.x
32. Cakmak I Horst WJ Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max) Physiol. Plant 1991 83 463 468 10.1111/j.1399-3054.1991.tb00121.x
Cakmak, I. & Horst, W. J. Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol. Plant 83, 463–468 (1991).10.1111/j.1399-3054.1991.tb00121.x
33. Mills, H. A. & Jones, J. B. Jr. Plant Analysis Handbook II: A Practical Sampling, Preparation, Analysis, and Interpretation Guide. Plant analysis handbook. A practical sampling, preparation, analysis, and interpretation guide. (Micro-Macro Publishing, Inc., USA, 1991).
34. Miller, R. Nitric-perchloric acid wet digestion in an open vessel. In Handbook of Reference Methods for Plant Analysis (ed. Kalra, Y.) 57–62 (CRC Press, Washington, D.C., 1997). 10.1201/9781420049398.ch6.
35. Estefan, G., Sommer, R. & Ryan, J. Methods of Soil, Plant , and Water Analysis : A Manual for the West Asia and North Africa Region. (International Center for Agricultural Research in the Dry Areas (ICARDA), Beirut, Lebanon, 2013).
36. Donald, A. H. & Hanson, D. Determination of potassium and sodium by flame emmision spectrophotometery. In Handbook of Reference Methods for Plant Analysis (ed. Kalra, Y.) 153–155 (CRC Press, Washington, D.C., 1998).
37. Pratt, P. F. Potassium. in Methods of Soil Analysis, Part 2: Chemical and Microbiological Properties (ed. Norman, A. G.) 1022–1030 (John Wiley & Sons, Ltd, Madison, WI, USA, 2016). 10.2134/agronmonogr9.2.c20.
38. Steel RG Torrie JH Dickey DA Principles and Procedures of Statistics: A Biometrical Approach 1997 McGraw Hill Book International Co.
Steel, R. G., Torrie, J. H. & Dickey, D. A. Principles and Procedures of Statistics: A Biometrical Approach (McGraw Hill Book International Co., 1997).
39. OriginLab Corporation. OriginPro. (OriginLab, Northampton, MA, USA., 2021).
40. Abenavoli MR Lupini A Oliva S Sorgonà A Allelochemical effects on net nitrate uptake and plasma membrane H+-ATPase activity in maize seedlings Biol. Plant 2010 54 149 153 10.1007/s10535-010-0024-0
Abenavoli, M. R., Lupini, A., Oliva, S. & Sorgonà, A. Allelochemical effects on net nitrate uptake and plasma membrane H+-ATPase activity in maize seedlings. Biol. Plant 54, 149–153 (2010).10.1007/s10535-010-0024-0
41. Zafar-ul-Hye M Nawaz MS Asghar H Waqas M Mahmood F Caffeic acid helps to mitigate adverse effects of soil salinity and other abiotic stresses in legume J. Genet. Genomes 2020 4 1 6
Zafar-ul-Hye, M., Nawaz, M. S., Asghar, H., Waqas, M. & Mahmood, F. Caffeic acid helps to mitigate adverse effects of soil salinity and other abiotic stresses in legume. J. Genet. Genomes 4, 1-6 (2020).
42. Perchlik M Tegeder M Improving plant nitrogen use efficiency through alteration of amino acid transport processes Plant Physiol. 2017 175 235 247 10.1104/pp.17.00608 28733388
Perchlik, M. & Tegeder, M. Improving plant nitrogen use efficiency through alteration of amino acid transport processes. Plant Physiol. 175, 235–247 (2017).28733388 10.1104/pp.17.00608
43. Kielland K Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling Ecology 1994 75 2373 2383 10.2307/1940891
Kielland, K. Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75, 2373–2383 (1994).10.2307/1940891
44. Gad, N. Interactive effect of salinity and cobalt on tomato plants. II. Some physiological parameters as affected by cobalt and salinity. Res. J. Agric. Biol. Sci. 1, 270–276 (2005).
45. Gad N Moez A Kandil H Response of Okra (Hibiscus esculentus) growth and productivity to cobalt and humic acid rates Int. J. Chem. Tech. Res. 2015 8 1782 1791
Gad, N., Moez, A. & Kandil, H. Response of Okra (Hibiscus esculentus) growth and productivity to cobalt and humic acid rates. Int. J. Chem. Tech. Res. 8, 1782–1791 (2015).
46. Gad N Role and importance of cobalt nutrition on groundnut (Arachis hypogaea) production World Appl. Sci. J. 2012 20 3 359 367
Gad, N. Role and importance of cobalt nutrition on groundnut (Arachis hypogaea) production. World Appl. Sci. J. 20(3), 359–367 (2012).
47. Gad N Role of cobalt on cowpea growth and yield under different levels of nitrogen World Appl. Sci. J. 2013 22 4 470 478
Gad, N. Role of cobalt on cowpea growth and yield under different levels of nitrogen. World Appl. Sci. J. 22(4), 470-478 (2013).
48. Singh A Tiwari S Pandey J Lata C Singh IK Role of nanoparticles in crop improvement and abiotic stress management J. Biotechnol. 2021 337 57 70 10.1016/j.jbiotec.2021.06.022 34175328
Singh, A., Tiwari, S., Pandey, J., Lata, C. & Singh, I. K. Role of nanoparticles in crop improvement and abiotic stress management. J. Biotechnol. 337, 57–70 (2021).34175328 10.1016/j.jbiotec.2021.06.022
49. Guha T Gopal G Mukherjee A Kundu R Fe3O4-urea nanocomposites as a novel nitrogen fertilizer for improving nutrient utilization efficiency and reducing environmental pollution Environ. Pollut. 2022 292 118301 10.1016/j.envpol.2021.118301 34626716
Guha, T., Gopal, G., Mukherjee, A. & Kundu, R. Fe3O4-urea nanocomposites as a novel nitrogen fertilizer for improving nutrient utilization efficiency and reducing environmental pollution. Environ. Pollut. 292, 118301 (2022).34626716 10.1016/j.envpol.2021.118301
50. Dimkpa CO Facile coating of urea with low-dose ZnO nanoparticles promotes wheat performance and enhances Zn uptake under drought stress Front. Plant. Sci. 2020 11 168 10.3389/fpls.2020.00168 32174943
Dimkpa, C. O. et al. Facile coating of urea with low-dose ZnO nanoparticles promotes wheat performance and enhances Zn uptake under drought stress. Front. Plant. Sci. 11, 168 (2020).32174943 10.3389/fpls.2020.00168
51. Beig B Development and testing of zinc sulfate and zinc oxide nanoparticle-coated urea fertilizer to improve N and Zn use efficiency Front. Plant Sci. 2023 13 1058219 10.3389/fpls.2022.1058219 36733597
Beig, B. et al. Development and testing of zinc sulfate and zinc oxide nanoparticle-coated urea fertilizer to improve N and Zn use efficiency. Front. Plant Sci. 13, 1058219 (2023).36733597 10.3389/fpls.2022.1058219
